Modelling the carbon balance in bryophytes and lichens: Presentation of PoiCarb 1.0, a new model for explaining distribution patterns and predicting climate-change effects.

PREMISE: Bryophytes and lichens have important functional roles in many ecosystems. Insight into their CO2 -exchange responses to climatic conditions is essential for understanding current and predicting future productivity and biomass patterns, but responses are hard to quantify at time scales beyond instantaneous measurements. We present PoiCarb 1.0, a model to study how CO2 -exchange rates of these poikilohydric organisms change through time as a function of weather conditions. METHODS: PoiCarb simulates diel fluctuations of CO2 exchange and estimates long-term carbon balances, identifying optimal and limiting climatic patterns. Modelled processes were net photosynthesis, dark respiration, evaporation and water uptake. Measured CO2 -exchange responses to light, temperature, atmospheric CO2 concentration, and thallus water content (calculated in a separate module) were used to parameterize the model's carbon module. We validated the model by comparing modelled diel courses of net CO2 exchange to such courses from field measurements on the tropical lichen Crocodia aurata. To demonstrate the model's usefulness, we simulated potential climate-change effects. RESULTS: Diel patterns were reproduced well, and the modelled and observed diel carbon balances were strongly positively correlated. Simulated warming effects via changes in metabolic rates were consistently negative, while effects via faster drying were variable, depending on the timing of hydration. CONCLUSIONS: Reproducing weather-dependent variation in diel carbon balances is a clear improvement compared to simply extrapolating short-term measurements or potential photosynthetic rates. Apart from predicting climate-change effects, future uses of PoiCarb include testing hypotheses about distribution patterns of poikilohydric organisms and guiding conservation strategies for species.

Relationships among sporophytic and gametophytic traits of 27 subtropical montane moss species.

PREMISE: Moss sporophytes differ strongly in size and biomass partitioning, potentially reflecting reproductive and dispersal strategies. Understanding how sporophyte traits are coordinated is essential for understanding moss functioning and evolution. This study aimed to answer: (1) how the size and proportions of the sporophyte differ between moss species with and without a prominent central strand in the seta, (2) how anatomical and morphological traits of the seta are related, and (3) how sporophytic biomass relates to gametophytic biomass and nutrient concentrations. METHODS: We studied the relationships between seta anatomical and morphological traits, the biomass of seta, capsule, and gametophyte, and carbon, nitrogen, and phosphorus concentrations of 27 subtropical montane moss species. RESULTS: (1) Moss species with a prominent central strand in the seta had larger setae and heavier capsules than those without a prominent strand. (2) With increasing seta length, setae became thicker and more rounded for both groups, while in species with a prominent central strand, the ratio of transport-cell area to epidermal area decreased. (3) In both groups, mosses with greater gametophytic biomass tended to have heavier sporophytes, but nitrogen and phosphorus concentrations in the gametophyte were unrelated to sporophytic traits. CONCLUSIONS: Our study highlights that the central strand in the seta may have an important functional role and affect the allometry of moss sporophytes. The coordinated variations in sporophyte morphological and anatomical traits follow basic biomechanical principles of cylinder-like structures, and these traits relate only weakly to the gametophytic nutrient concentrations. Research on moss sporophyte functional traits and their relationships to gametophytes is still in its infancy but could provide important insights into their adaptative strategies.

A research agenda for nonvascular photoautotrophs under climate change.

Nonvascular photoautotrophs (NVP), including bryophytes, lichens, terrestrial algae, and cyanobacteria, are increasingly recognized as being essential to ecosystem functioning in many regions of the world. Current research suggests that climate change may pose a substantial threat to NVP, but the extent to which this will affect the associated ecosystem functions and services is highly uncertain. Here, we propose a research agenda to address this urgent question, focusing on physiological and ecological processes that link NVP to ecosystem functions while also taking into account the substantial taxonomic diversity across multiple ecosystem types. Accordingly, we developed a new categorization scheme, based on microclimatic gradients, which simplifies the high physiological and morphological diversity of NVP and world-wide distribution with respect to several broad habitat types. We found that habitat-specific ecosystem functions of NVP will likely be substantially affected by climate change, and more quantitative process understanding is required on: (1) potential for acclimation; (2) response to elevated CO2 ; (3) role of the microbiome; and (4) feedback to (micro)climate. We suggest an integrative approach of innovative, multimethod laboratory and field experiments and ecophysiological modelling, for which sustained scientific collaboration on NVP research will be essential.

Simulating climate change in situ in a tropical rainforest understorey using active air warming and CO2 addition.

Future climate-change effects on plant growth are most effectively studied using microclimate-manipulation experiments, the design of which has seen much advance in recent years. For tropical forests, however, such experiments are particularly hard to install and have hence not been widely used. We present a system of active heating and CO2 fertilization for use in tropical forest understoreys, where passive heating is not possible. The system was run for 2 years to study climate-change effects on epiphytic bryophytes, but is also deemed suitable to study other understorey plants. Warm air and CO2 addition were applied in 1.6-m-tall, 1.2-m-diameter hexagonal open-top chambers and the microclimate in the chambers compared to outside air. Warming was regulated with a feedback system while CO2 addition was fixed. The setup successfully heated the air by 2.8 K and increased CO2 by 250 ppm on average, with +3 K and +300 ppm as the targets. Variation was high, especially due to technical breakdowns, but not biased to times of the day or year. In the warming treatment, absolute humidity slightly increased but relative humidity dropped by between 6% and 15% (and the vapor pressure deficit increased) compared to ambient, depending on the level of warming achieved in each chamber. Compared to other heating systems, the chambers provide a realistic warming and CO2 treatment, but moistening the incoming air would be needed to avoid drying as a confounding factor. The method is preferable over infrared heating in the radiation-poor forest understorey, particularly when combined with CO2 fertilization. It is suitable for plant-level studies, but ecosystem-level studies in forests may require chamber-less approaches like infrared heating and free-air CO2 enrichment. By presenting the advantages and limitations of our approach, we aim to facilitate further climate-change experiments in tropical forests, which are urgently needed to understand the processes determining future element fluxes and biodiversity changes in these ecosystems.

Global maps of soil temperature.

Research in global change ecology relies heavily on global climatic grids derived from estimates of air temperature in open areas at around 2 m above the ground. These climatic grids do not reflect conditions below vegetation canopies and near the ground surface, where critical ecosystem functions occur and most terrestrial species reside. Here, we provide global maps of soil temperature and bioclimatic variables at a 1-km2 resolution for 0-5 and 5-15 cm soil depth. These maps were created by calculating the difference (i.e. offset) between in situ soil temperature measurements, based on time series from over 1200 1-km2 pixels (summarized from 8519 unique temperature sensors) across all the world's major terrestrial biomes, and coarse-grained air temperature estimates from ERA5-Land (an atmospheric reanalysis by the European Centre for Medium-Range Weather Forecasts). We show that mean annual soil temperature differs markedly from the corresponding gridded air temperature, by up to 10°C (mean = 3.0 ± 2.1°C), with substantial variation across biomes and seasons. Over the year, soils in cold and/or dry biomes are substantially warmer (+3.6 ± 2.3°C) than gridded air temperature, whereas soils in warm and humid environments are on average slightly cooler (-0.7 ± 2.3°C). The observed substantial and biome-specific offsets emphasize that the projected impacts of climate and climate change on near-surface biodiversity and ecosystem functioning are inaccurately assessed when air rather than soil temperature is used, especially in cold environments. The global soil-related bioclimatic variables provided here are an important step forward for any application in ecology and related disciplines. Nevertheless, we highlight the need to fill remaining geographic gaps by collecting more in situ measurements of microclimate conditions to further enhance the spatiotemporal resolution of global soil temperature products for ecological applications.

Desert breath-How fog promotes a novel type of soil biocenosis, forming the coastal Atacama Desert's living skin.

The Atacama Desert is the driest non-polar desert on Earth, presenting precarious conditions for biological activity. In the arid coastal belt, life is restricted to areas with fog events that cause almost daily wet-dry cycles. In such an area, we discovered a hitherto unknown and unique ground covering biocenosis dominated by lichens, fungi, and algae attached to grit-sized (~6 mm) quartz and granitoid stones. Comparable biocenosis forming a kind of a layer on top of soil and rock surfaces in general is summarized as cryptogamic ground covers (CGC) in literature. In contrast to known CGC from arid environments to which frequent cyclic wetting events are lethal, in the Atacama Desert every fog event is answered by photosynthetic activity of the soil community and thus considered as the desert's breath. Photosynthesis of the new CGC type is activated by the lowest amount of water known for such a community worldwide thus enabling the unique biocenosis to fulfill a variety of ecosystem services. In a considerable portion of the coastal Atacama Desert, it protects the soil from sporadically occurring splash erosion and contributes to the accumulation of soil carbon and nitrogen as well as soil formation through bio-weathering. The structure and function of the new CGC type are discussed, and we suggest the name grit-crust. We conclude that this type of CGC can be expected in all non-polar fog deserts of the world and may resemble the cryptogam communities that shaped ancient Earth. It may thus represent a relevant player in current and ancient biogeochemical cycling.

Associations between shoot-level water relations and photosynthetic responses to water and light in 12 moss species.

In vascular plants, there is a clear coupling between traits related to water and traits related to carbon economics. For bryophytes this coupling has been little studied but is expected to be strong, because in these poikilohydric plants photosynthesis varies strongly with water availability. We hypothesized that there is a trade-off between water-holding and photosynthetic capacities for mosses, resulting in a limited spectrum of possible trait combinations. At one end of this spectrum, mosses would tend to stay wet and active for long periods but would have slow photosynthetic rates. At the other end, mosses would avoid external water and dry out quicker but would have high photosynthetic capacities. We determined the water relations (water-holding and -retention capacities), photosynthetic water- and light-response curves of shoots of 12 moss species and explored the associations between these traits and their distributions among the studied species. The results partly support our hypotheses, in that the water-holding and water-retention capacities of mosses are positively related to each other and to the value and width of the optimal water-content range for photosynthesis. However, the photosynthetic capacities were specific to taxonomic groups, and the relationships between the water relations and the photosynthetic capacity are weak or inconsistent and depend strongly on the species used for analysis. The positive relationships between water-holding, water-retention and photosynthetic water-use capacities suggest two contrasting adaptations to avoid damage during dehydration: taking more time to 'prepare' or quick photosynthetic adjustment. However, the spectrum we hypothesized cannot be generalized for all mosses and defining a broader spectrum will require the extension of this study to a much larger number of species and including stand-level measurements of water loss and photosynthesis.

Comparisons of photosynthesis-related traits of 27 abundant or subordinate bryophyte species in a subalpine old-growth fir forest.

Bryophyte communities can exhibit similar structural and taxonomic diversity as vascular plant communities, just at a smaller scale. Whether the physiological diversity can be similarly diverse, and whether it can explain local abundance patterns is unknown, due to a lack of community-wide studies of physiological traits. This study re-analyzed data on photosynthesis-related traits (including the nitrogen, phosphorus and chlorophyll concentrations, photosynthetic capacities, and photosynthetic nutrient use efficiencies) of 27 bryophyte species in a subalpine old-growth fir forest on the eastern Tibetan Plateau. We explored differences between taxonomic groups and hypothesized that the most abundant bryophyte species had physiological advantages relative to other subdominant species. Principal component analysis (PCA) was used to summarize the differences among species and trait values of the most abundant and other co-occurring subdominant species. Species from the Polytrichaceae were separated out on both PCA axes, indicating their high chlorophyll concentrations and photosynthetic capacities (axis 1) and relatively high-light requirements (axis 2). Mniaceae species also had relatively high photosynthetic capacities, but their light saturation points were low. In contrast, Racomitrium joseph-hookeri and Lepidozia reptans, two species with a high shoot mass per area, had high-light requirements and low nutrient and chlorophyll concentrations and photosynthetic capacities. The nutrient concentrations, photosynthetic capacities, and photosynthetic nutrient use efficiencies of the most abundant bryophyte species did not differ from co-occurring subdominant species. Our research confirms the links between the photosynthesis-related traits and adaptation strategies of bryophytes. However, species relative abundance was not related to these traits.

The 'plant economic spectrum' in bryophytes, a comparative study in subalpine forest.

PREMISE OF THE STUDY: Tradeoffs among functional traits of vascular plants are starting to be better understood, but it is unclear whether bryophytes possess similar tradeoffs or how trait relationships, or the 'economic spectrum', differ between the two groups. METHODS: We determined functional-trait values [including shoot mass per area (SMA), light-saturated assimilation rate (Amass), dark respiration rate (Rdmass), N and P concentrations (Nmass and Pmass), and photosynthetic N and P use efficiency (PNUE and PPUE)] and their bivariate relationships for 28 bryophytes growing in a subalpine old-growth fir forest on the eastern Tibetan Plateau. Trait values and scaling relationships of these bryophytes were compared with data for vascular plant leaves from the Global Plant Trait Network (GLOPNET) dataset. KEY RESULTS: We found that the Amass, Nmass, N:P, PNUE and PPUE of bryophyte shoots were lower than those of vascular plant leaves. In contrast, bryophytes possessed higher Pmass and the two groups had similar values of SMA and Rdmass. The Nmass and Pmass were closely associated with Amass and Rdmass, and these traits were all significantly negatively related to SMA. Metabolic rates increased faster with nutrient concentrations in bryophytes than in vascular plants. CONCLUSIONS: Our research indicates that bryophytes have similar trait relationships as vascular plant leaves, although the slopes of the relationships differ for most trait combinations. This study confirms a functional-trait tradeoff in bryophytes, and reveals that bryophytes allocate greater proportions of N and P into the metabolic pools.

Carbohydrate reserves in the facilitator cushion plant Laretia acaulis suggest carbon limitation at high elevation and no negative effects of beneficiary plants.

The elevational range of the alpine cushion plant Laretia acaulis (Apiaceae) comprises a cold upper extreme and a dry lower extreme. For this species, we predict reduced growth and increased non-structural carbohydrate (NSC) concentrations (i.e. carbon sink limitation) at both elevational extremes. In a facilitative interaction, these cushions harbor other plant species (beneficiaries). Such interactions appear to reduce reproduction in other cushion species, but not in L. acaulis. However, vegetative effects may be more important in this long-lived species and may be stronger under marginal conditions. We studied growth and NSC concentrations in leaves and stems of L. acaulis collected from cushions along its full elevational range in the Andes of Central Chile. NSC concentrations were lowest and cushions were smaller and much less abundant at the highest elevation. At the lowest elevation, NSC concentrations and cushion sizes were similar to those of intermediate elevations but cushions were somewhat less abundant. NSC concentrations and growth did not change with beneficiary cover at any elevation. Lower NSC concentrations at the upper extreme contradict the sink-limitation hypothesis and may indicate that a lack of warmth is not limiting growth at high-elevation. At the lower extreme, carbon gain and growth do not appear more limiting than at intermediate elevations. The lower population density at both extremes suggests that the regeneration niche exerts important limitations to this species' distribution. The lack of an effect of beneficiaries on reproduction and vegetative performance suggests that the interaction between L. acaulis and its beneficiaries is probably commensalistic.

Early establishment of trees at the alpine treeline: idiosyncratic species responses to temperature-moisture interactions.

On a global scale, temperature is the main determinant of arctic and alpine treeline position. However on a local scale, treeline form and position vary considerably due to other climatic factors, tree species ecology and life-stage-dependent responses. For treelines to advance poleward or uphill, the first steps are germination and seedling establishment. These earliest life stages may be major bottlenecks for treeline tree populations and will depend differently on climatic conditions than adult trees. We investigated the effect of soil temperature and moisture on germination and early seedling survival in a field experiment in the French Alps near the local treeline (2100 m a.s.l.) using passive temperature manipulations and two watering regimes. Five European treeline tree species were studied: Larix decidua, Picea abies, Pinus cembra, Pinus uncinata and Sorbus aucuparia In addition, we monitored the germination response of three of these species to low temperatures under controlled conditions in growth chambers. The early establishment of these trees at the alpine treeline was limited either by temperature or by moisture, the sensitivity to one factor often depending on the intensity of the other. The results showed that the relative importance of the two factors and the direction of the effects are highly species-specific, while both factors tend to have consistent effects on both germination and early seedling survival within each species. We show that temperature and water availability are both important contributors to establishment patterns of treeline trees and hence to species-specific forms and positions of alpine treelines. The observed idiosyncratic species responses highlight the need for studies including several species and life-stages to create predictive power concerning future treeline dynamics.

A cool experimental approach to explain elevational treelines, but can it explain them?

At alpine treeline, trees give way to low-stature alpine vegetation. The main reason may be that tree canopies warm up less in the sun and experience lower average temperatures than alpine vegetation. Low growth temperatures limit tissue formation more than carbon gain, but whether this mechanism universally determines potential treeline elevations is the subject of debate. To study low-temperature limitation in two contrasting treeline tree species, Fajardo and Piper (American Journal of Botany 101: 788-795) grew potted seedlings at ground level or suspended at tree-canopy height (2 m), introducing a promising experimental method for studying the effects of alpine-vegetation and tree-canopy microclimates on tree growth. On the basis of this experiment, the authors concluded that lower temperatures at 2 m caused carbon limitation in one of the species and that treeline-forming mechanisms may thus be taxon-dependent. Here we contest that this important conclusion can be drawn based on the presented experiment, because of confounding effects of extreme root-zone temperature fluctuations and potential drought conditions. To interpret the results of this elegant experiment without logistically challenging technical modifications and to better understand how low temperature leads to treeline formation, studies on effects of fluctuating vs. stable temperatures are badly needed. Other treeline research priorities are interactions between temperature and other climatic factors and differences in microclimate between tree canopies with contrasting morphology and physiology. In spite of our criticism of this particular study, we agree that the development of a universal treeline theory should include continuing explorations of taxon-specific treeline-forming mechanisms.

Altitudinal changes in temperature responses of net photosynthesis and dark respiration in tropical bryophytes.

BACKGROUND AND AIMS: There is a conspicuous increase of poikilohydric organisms (mosses, liverworts and macrolichens) with altitude in the tropics. This study addresses the hypothesis that the lack of bryophytes in the lowlands is due to high-temperature effects on the carbon balance. In particular, it is tested experimentally whether temperature responses of CO(2)-exchange rates would lead to higher respiratory carbon losses at night, relative to potential daily gains, in lowland compared with lower montane forests. METHODS: Gas-exchange measurements were used to determine water-, light-, CO(2)- and temperature-response curves of net photosynthesis and dark respiration of 18 tropical bryophyte species from three altitudes (sea level, 500 m and 1200 m) in Panama. KEY RESULTS: Optimum temperatures of net photosynthesis were closely related to mean temperatures in the habitats in which the species grew at the different altitudes. The ratio of dark respiration to net photosynthesis at mean ambient night and day temperatures did not, as expected, decrease with altitude. Water-, light- and CO(2)-responses varied between species but not systematically with altitude. CONCLUSIONS: Drivers other than temperature-dependent metabolic rates must be more important in explaining the altitudinal gradient in bryophyte abundance. This does not discard near-zero carbon balances as a major problem for lowland species, but the main effect of temperature probably lies in increasing evaporation rates, thus restricting the time available for photosynthetic carbon gain, rather than in increasing nightly respiration rates. Since optimum temperatures for photosynthesis were so fine tuned to habitat temperatures we analysed published temperature responses of bryophyte species worldwide and found the same pattern on the large scale as we found along the tropical mountain slope we studied.